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J. Biol. Chem., Vol. 281, Issue 16, 11214-11224, April 21, 2006

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Stomach-specific Calpain, nCL-2, Localizes in Mucus Cells and Proteolyzes the -Subunit of Coatomer Complex, -COP^*

Shoji Hata, Suguru Koyama, Hiroyuki Kawahara^¶, Naoko Doi^||, Tatsuya Maeda^||**, Noriko Toyama-Sorimachi, Keiko Abe, Koichi Suzuki, and Hiroyuki Sorimachi^||1

From the Department of Enzymatic Regulation for Cell Functions, The Tokyo Metropolitan Institute of Medical Science (Rinshoken), Tokyo 113-8613, the Graduate School of Agricultural and Life Sciences, the University of Tokyo, Tokyo 113-8657, the ^¶Graduate School of Pharmaceutical Sciences, Hokkaido University, Hokkaido 060-0812, ^||CREST, Japan Science and Technology, Saitama 332-0012, the ^**Institute of Molecular and Cellular Biosciences, the University of Tokyo, Tokyo 113-0032, the Department of Gastroenterology, Research Institute, International Medical Center of Japan, Tokyo 162-8655, and the New Frontiers Research Laboratories, Toray Industries Inc., Kanagawa 248-8555, Japan

Calpain is a Ca²⁺-regulated cytosolic protease. Mammals have 14 calpain genes, half of which are predominantly expressed in specific organ(s); the rest are expressed ubiquitously. A defect in calpains causes lethality/pathogenicity, indicating their physiological indispensability. nCL-2/calpain-8a was identified as a stomach-specific calpain, whose physiological functions are unclear. To elucidate these, we characterized nCL-2 in detail. Unexpectedly, nCL-2 was localized strictly to the surface mucus cells in the gastric epithelium and the mucus-secreting goblet cells in the duodenum. Yeast two-hybrid screening identified several nCL-2-intracting molecules. Of these, the -subunit of coatomer complex (-COP) occurs in the stomach pit cells and is proteolyzed by nCL-2 in vitro. Furthermore, -COP and nCL-2 co-expressed in COS7 cells co-localized in the Golgi, and Ca²⁺-ionophore stimulation caused the proteolysis of -COP near the linker region, resulting in the dissociation of -COP from the Golgi. These results strongly suggest novel functions for nCL-2 that involve the membrane trafficking of mucus cells via interactions with coat protein.

Received for publication, August 22, 2005 , and in revised form, December 27, 2005.

^* This work was supported in part by MEXT.KAKENHI 16026209 (to H. S.), 14704064, 15032201, and 16026201 (to H. K.), 14086203 (to T. M.), 14380309 (to K. S.), and 14656054 (to K. A.), by JSPS.KAKENHI 15380089 (to H. S.) and 02J07250 (to S. H.), by a Research Grant (14B-4) for Nervous and Mental Disorders from the Ministry of Health, Labor and Welfare, and by Ground-Based Research Announcement for Space Utilization promoted by Japan Space Forum (to H. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Tel./Fax: 81-3-3823-2181; E-mail: sorimach{at}rinshoken.or.jp.

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